THE CRUSTACEAN INTEGUMENT: SETAE

6 THE CRUSTACEAN INTEGUMENT: SETAE, SETULES, AND OTHER ORNAMENTATION

Anders Garm and Les Watling

Abstract The cuticle plays an important role in many aspects of crustacean biology, since it is the interface to the surrounding world. Thus, the cuticle displays many structural specializations all over the body. The structures considered here are setae, setules, denticles, and spines. We provide definitions for them and discuss their functional morphology and development, with the main focus on setae. We recognize seven types of setae based on their detailed external morphology: plumose, pappose, composite, serrate, papposerrate, simple, and cuspidate. In support of the categorization of these setae, each seems to correlate with a specific functional outcome such as feeding, grooming, and locomotion. Setae are also important sensory organs, and in crustaceans they are normally bimodal chemo- and mechanoreceptors, but there are also indications of thermo-, osmo-, and hygrosensitivity. Little can be learned about the sensory functions from the external morphology of setae, but their ultrastructure seems to provide better cues. In particular, mechanoreceptors display structures related to transduction mechanisms, with the scolopale as a good example. Still, too few data are available outside malacostracans to draw general conclusions for all crustaceans, underlining the need for multidisciplinary and broad intertaxon studies. Less is known about the functional morphology and development of setules and denticles in the general cuticle, but they seem to be homologous with similar structures on the setae. Arthropods outside Crustacea also have setae in their cuticle, and many shared features can be found. They are especially well studied in insects, where many correlations between structure and function have been shown.

INTRODUCTION TO THE STRUCTURES OF THE CRUSTACEAN CUTICLE: DEFINITIONS/CLASSIFICATION One of the defining characters of crustaceans as well as other arthropods is their external skeleton, the cuticle (see also chapter 5). The cuticle plays a major role in most aspects of crustacean Functional Morphology and Diversity. Edited by Les Watling and Martin Thiel. © 2013 Oxford University Press. Published 2013 by Oxford University Press.

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Functional Morphology and Diversity biology, and this has led to a vast number of structural and functional specializations. Many of these specializations lie within the detailed surface structures, and they are the topic of this chapter. First, we provide an overview of the diversity of these structures and their functions and use this to suggest a classification system. The main part of the review then focuses in detail on the major group of cuticular specializations, the setae, since they are by far the most studied and have the greatest functional diversity and importance. We end by comparing with data from other arthropod groups and listing suggestions for where future research in this field is most needed and will be most fruitful. When observing crustaceans with the naked eye, many of the cuticular specializations are visible in a large number of species (Fig. 6.1A). Some body parts and especially the appendages appear furry (Fig. 6.1B), and the hairlike structures found in these areas are outgrowths of the general cuticle, normally with a distinct articulation at the base, making them flexible (Figs. 6.1D, 6.2). There is a general consensus that these structures are homologous within Crustacea and are also probably homologous with similar structures in other arthropods. Many terms have been used for these structures, such as setae, sensilla, bristles, or even “hairs.” For crustaceans, the most often used term is setae, and it will therefore be used here. Even though setae are in general considered homologous, it is difficult to decide which cuticular projections to include in this term. A number of authors have addressed this problem and provided definitions of what they considered setae. Thomas (1970) was one of the first to do so, and he proposed that all elongate outgrowths with distal pores were setae. His work was based on light microscopy, and electron microscopy work has since shown his definition to be far too narrow. Fish (1972) considered elongate outgrowths filled with “cytoplasm” as setae, but this very broad definition will include many other structures, such as spines (see below), and exclude setae with no cells in the lumen. Some authors have used the size of the cuticular structures as a basis for classification. This has led to such terms as microsetae (Jacques 1989) and microtrichs (Cuadras 1982, Steele and Steele 1997, 1999), but we do not approve of this approach. If a structure complies with our given definition (see below), we will consider it a seta no matter the size, and we see no reason to believe that they cannot be small. In fact, we believe that in small crustaceans, such as nauplius larvae, there has been strong selection pressure for miniaturizing the setae. An evolutionary perspective was taken by Watling (1989), who stressed the need for a definition based on homologies. He suggested that the articulation with the general cuticle is such a homology and used this structure to define setae from other cuticular outgrowths. This definition has been widely accepted as it seems to hold true for the vast majority of setae, and the “stem seta” probably also had such an articulation. When considering the diversity of present-day crustaceans, though, Watling’s definition runs into some problems, which were first addressed in an earlier review (Garm 2004b). Some of the articulated outgrowths have an external and internal morphology so similar to long setules found on some of the setae that there are no structural arguments to consider them as being different. They are commonly found on the mouthparts of decapods and peracarids (Fig. 6.1C), and we suggest that they should be included in the term setules (see below). The other problem concerns a loss of the articulation between the setae and the general cuticle. This has probably happened a number of times in several crustacean lineages to encompass mechanical functions requiring a very sturdy seta (Garm and Høeg 2001, Garm 2004a). Clear examples of such loss are seen for the spinelike projection found on the basis of maxilla 1 of the squat lobster Munida sarsi (Fig. 6.2B). These unarticulated projections are innervated, have a continuous lumen, and have a cellular arrangement very similar to other setae. Further, structures undoubtedly homologous with the spinelike projections (they are situated in the same place and arranged in the same two parallel rows in other decapod species) are typical setae with clear articulation (Garm 2004b). The same situation is seen for unarticulated spinelike

Setae, Setules, and Other Ornamentation

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Fig. 6.1. Structures in the crustacean cuticle. (A) At the macroscopic level, many crustaceans, such as the hermit crab Parapagurus sulcata, appear furry because of very heavy setation (picture courtesy of Dr. Jens T. Høeg). (B) Maxilliped 1 of the hermit crab Pagurus bernhardus displaying heavy setation, especially on the medial edges of the coxa and basis. Several types of setae are present. (C) Setules from paragnath of P. bernhardus are clearly articulated with the general cuticle (inset). (D) Between the setae (S) on the mouthpart of Panulirus argus, the cuticle is filled with teethlike structures (denticles). (E) Ultrastructure of setules from the paragnath of Penaeus monodon shows that they are made entirely of cuticle and lack a lumen and innervation. (F) Ultrastructure of setae show a round, hollow base filled with sheath cells (ShC). Cu, setal cuticle. (G) Close-up of the central part of the setal lumen showing that the semicircular sheath cells (ShC) encircle the outer dendritic segments (ODS) of a number of sensory cells.

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Fig. 6.2. Details of the external morphology of setae. (A) Spinelike setae from maxilla 1 of Munida sarsi, with no apparent articulation at the base (arrows). (B) Plumose setae displaying a supracuticular articulation (arrows) with the general cuticle, making them very flexible. (C) Most setae have an infracuticular articulation (arrows) with the general cuticle, reducing their flexibility. (D) Setules from a composite seta showing an articulation (arrows) with the setal shaft. (E) Some setae display unarticulated teethlike structures arranged parallel to the setal shaft. These denticles (De) are found in two rows on the distal half of the setae often together with small setules (S). (F) On some setae, there is a graduated transformation between setules (S) and denticles (De). (G) Many setae display a terminal pore (TP) at the tip, often associated with small scalelike setules. (H) The tip of a seta used for grooming the gills. Such setae often have a specialized tip. (I) A newly molted composite seta displaying a very distinct annulus (ringed) as a by-product from the invagination during development.

Setae, Setules, and Other Ornamentation setae on the dactylus of maxilliped 3 of the shrimp Palaemon adspersus. The definition we will follow here was put forward by Garm (2004b, 1): “A seta is an elongate projection with a more or less circular base and a continuous lumen. The lumen has a semicircular arrangement of sheath cells basally.” The available data on the ultrastructure of setae provide good support for the internal characteristics—the continuous lumen and the semicircular sheath cells (Fig. 6.1F,G), also called enveloping cells (Alexander et al. 1980, Hallberg et al. 1992, Crouau 1997, Paffenhöfer and Loyd 2000). That the sheath cells seem to be a unifying character for setae indicates that they play important functional roles. They are involved in setal development, and this complex process could possibly provide a more detailed definition. The continuous lumen is also functionally significant since it is closely connected with the sensory properties of setae. Both of these topics are discussed in detail in later sections. It is often problematic to use internal characters because categorization is normally based on light or scanning electron microscopy. The round shape of the basal part of a seta is therefore an important character, and it seems to be very consistent for setae found on all body parts of many groups of crustaceans (see Garm 2004b for review). Still, using this character alone will not suffice since it will not separate unarticulated setae and spines dealt with below. Besides setae, there are other surface structures of the cuticle that we will briefly consider. One group has already been mentioned—the setules. As said above, this is a term widely used for certain outgrowths on setae, but we believe them to be a general feature of the cuticle. They are elongate structures, 10–150 μm long, often inserted into the cuticle in a socket, making them flexible (Fig. 6.1C). They are flattened in cross section and made entirely of cuticle, so they are never innervated and do not contain semicircular sheath cells basally (Fig. 6.1E). Most often they have a serrated edge distally. Such setules are commonly found in the general cuticle throughout the Crustacea, especially on the mouth apparatus and in the foregut, but they have typically been referred to as setae (Halcrow and Bousfield 1987, Holmquist 1989, Martin 1989, Olesen 2001). Another expression often used when describing the cuticle of crustacean is denticles. Like setules, denticles are commonly found on setae but also in the general cuticle. This again stresses that some of the structures generally considered special features of setae are in fact general cuticular characteristics. Denticles are relatively small structures (normally < 30 μm long) and, as the name implies, more or less tooth shaped (Fig. 6.1D). They are unarticulated, made entirely of cuticle, and never innervated. There is some evidence that they are in fact evolutionarily related to setules (Garm 2004b). A common cuticular outgrowth is the spine. This term should be used with care since it can be very hard to tell a true spine from an unarticulated seta. We consider a spine to be an unarticulated extension of the general cuticle. It is hollow, and the lumen is lined with normal epithelial cells; no innervation is present unless the spine carries setae (see, e.g., Martin and Cash-Clark 1995, their fig. 19A,C). If ultrastructural data are not available, then comparison with closely related species should be used to verify that they do not have setae in the same position. While the other types of structures are probably homologies, we find it very likely that spines have arisen several times and represent convergent evolution. Scales, like spines, are cuticular outgrowths, but they are generally wider than long and are not usually hollow (Klepal and Kastner 1980). Most often, scales follow one side of the outline of the polygons often visible on crustacean cuticles when observed with the scanning electron microscope. While it was long known that the crustacean cuticle was often sculptured, the exact details could not be seen until the invention of the scanning electron microscope. Some of the main features are summarized by Meyer-Rochow (1980), Holdich (1984), and Halcrow

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Functional Morphology and Diversity and Bousfield (1987). A terminology of surface sculpturing was proposed by Harris (1979) for insects, but it seems equally applicable to crustaceans. The basic unit of sculpturing seems to be a more or less well-defined polygon, which Hinton (1970) and Duncan (1985) assert represents the surface mani festation of underlying epidermal cells (see also chapter 5). Scales, microspines, micropores, and a large variety of other structures can be found within and along the boundaries of polygons (e.g., Klepal and Kastner 1980, Halcrow and Bousfield 1987). In many other crustaceans and insects, however, the polygon is obliterated by cuticular secretions that form more elaborate sculpture (e.g., Hinton 1970, MeyerRochow 1980).

THE EXTERNAL STRUCTURE OF SETAE As discussed in the preceding section, setae constitute the largest and most diverse group of structures, which is also why providing a general definition is not a trivial task. This diversity is seen between species, but sometimes a single species carries close to the full diversity of seta types. Most of the setae are found on the appendages, and especially the mouthparts are heavily ornamented with setae, and a single segment (= article) of, for example, a maxilliped can display quite a number of setal types (Fig. 6.1B). In the following we will try to deconstruct this diversity and pinpoint some of the important structures that cause the diversity. Structures that share some kind of similarities can be a product of the evolutionary history of setae and thereby be considered homologies, and/or they can be products of shared functionality. As we discuss further below, most of the similarities of setae stem from shared functions, and this will be used to suggest a classification system. First, it is important to recognize that all setae can be seen as having a more or less elongate and round (at least at the base) central part, the shaft, which may or may not have specializations, including different types of outgrowths. The length of the shaft varies from just a few micrometers to several millimeters in large decapods. They are found on all body parts, including internally in the foregut (Altner et al. 1986, Johnston 1999), and serve many different functions. This diversity of function has undoubtedly added to the wide range of external morphology. Some setae are long and slender with no apparent specializations along the setal shaft (Fig. 6.2F,G), whereas others have many types of outgrowths, resembling feathers or pine trees (Fig. 6.2A,B). Still others are thorn shaped or bent and appear as hooks. Despite the diversity, several substructures can be recognized in many setae and can be used to group the setae into different types. If a classification includes too many details, there is a high risk that the designated setal types will be highly specialized and appear only in a very limited number of taxa. Here, we try to avoid this problem and consider only overall structural similarities found in most major crustacean taxa, since this will have the broadest application and interest. One of the prominent substructures concerns how the setae attach to the general cuticle. Three types of attachments are seen: (1) an articulation in the form of a socket, which is drawn into the general cuticle and gives the seta an infracuticular articulation (Fig. 6.3C)—this is by far the most common type of attachment; (2) the socket is extended from the general cuticle, giving the seta a supracuticular articulation (Fig. 6.3B)—this gives the seta great flexibility and is often seen in setae experiencing large drag forces; (3) no articulation is seen, and the general cuticle has a direct transition into the cuticle of the seta (Fig. 6.3A)—as mentioned earlier, the articulation is probably reduced to obtain sturdiness. Another feature concerning the sturdiness is the length:width (L:W) ratio of the shaft, where the width is measured at the base of the seta. The vast majority of setae are slim, with a L:W ratio of >15 (Fig. 6.2), but some setae are more stout and robust, with a L:W ratio 15 – Infra – + – >15 Ter/– Infra – +/– + >15 Ter/ Sub/– Infra + +/– + >15 Ter/– Infra – – – >15 Ter/– Infra/absent – +/– –